Plant-parasitic nematodes: towards understanding molecular players in stress responses

Abstract

Background Plant–parasitic nematode interactions occur within a vast molecular plant immunity network. Following initial contact with the host plant roots, plant-parasitic nematodes (PPNs) activate basal immune responses. Defence priming involves the release in the apoplast of toxic molecules derived from reactive species or secondary metabolism. In turn, PPNs must overcome the poisonous and stressful environment at the plant–nematode interface. The ability of PPNs to escape this first line of plant immunity is crucial and will determine its virulence. Scope Nematodes trigger crucial regulatory cytoprotective mechanisms, including antioxidant and detoxification pathways. Knowledge of the upstream regulatory components that contribute to both of these pathways in PPNs remains elusive. In this review, we discuss how PPNs probably orchestrate cytoprotection to resist plant immune responses, postulating that it may be derived from ancient molecular mechanisms. The review focuses on two transcription factors, DAF-16 and SKN-1, which are conserved in the animal kingdom and are central regulators of cell homeostasis and immune function. Both regulate the unfolding protein response and the antioxidant and detoxification pathways. DAF-16 and SKN-1 target a broad spectrum of Caenorhabditis elegans genes coding for numerous protein families present in the secretome of PPNs. Moreover, some regulatory elements of DAF-16 and SKN-1 from C. elegans have already been identified as important genes for PPN infection. Conclusion DAF-16 and SKN-1 genes may play a pivotal role in PPNs during parasitism. In the context of their hub status and mode of regulation, we suggest alternative strategies for control of PPNs through RNAi approaches.

Metabolomics as an Emerging Tool for the Study of Plant–Pathogen Interactions

“…Plant nematodes are obligate soilborne pathogens that infect plant roots. They have evolved sophisticated mechanisms for parasitism, with different feeding stylets and effector secretion for host manipulation [115,116]. They can be roughly divided into three main categories, according to the symptoms induced in their hosts: i) Cyst nematodes are associated with the sedentary genera Heterodera and Globodera; ii) root-knots are mostly caused by the sedentary species of Meloidogyne genus; and iii) lesions are mainly associated with the migratory endoparasitic genus Pratylenchus [117].…”

MiDaf16-like and MiSkn1-like gene families are reliable targets to develop biotechnological tools for the control and management of Meloidogyne incognita

“…Genome and transcriptome studies from PPNs have revealed genes orthologous to Daf-16 and Skn-1 from C. elegans in the Meloidogyne, Pratylenchus, and Bursaphelenchus genera 39,[58][59][60] . The high level of sequence conservation suggests similar functions to those observed in C. elegans 13,35,59 . Studies of comparative genomes in PPNs have identified numerous defense genes from the DAF-16 and SKN-1 networks involved in ROS scavenging, coding proteins linked to the antioxidant pathway, superoxide dismutases (SOD), catalases (CAT), glutathione S-transferases (GST), glutathione peroxidase (GPX), and peroxiredoxins (PRDX) 11,18,20,58,61 .…”

“…On the other hand, the 14-3-3 scaffolding proteins bind to the phosphorylation sites of DAF-16 and contribute to its sequestration within the cytoplasm 51,52 . In the nucleus, the DAF-16 and SKN-1 TFs are responsible for the transcriptional activation of up to 500 and 846 genes, respectively 13,53 . These activated genes belong to several functional groups and are implicated in the aging and longevity process and the antioxidant, detoxification, and protein unfolding response pathways [54][55][56][57] .…”

“…Interestingly, without targeting all the members of these families because they are highly conserved in nematodes and other animals, these two gene families may be potential targets for the development of NBTs to impair the defense pathways of PPNs during plant parasitism. M. incognita is a RKN 10 , an important plant pathogen causing economic losses in several crops worldwide 11 , and an excellent model system for obligate sedentary endoparasitic PPNs 13,21 . Our findings confirm that in planta downregulation of MiDaf16-like1, MiSkn1-like1 (single-gene silencing), or both genes simultaneously (double-gene silencing), makes nematodes more susceptible to stress conditions during parasitism, significantly reducing the number of galls and eggs, NRF, and, consequently, decreasing the source of inoculum.…”

“…Thus, the use of this biotechnological strategy is of great relevance in crops or cultivars of economic interest (such as soybean, cotton, coffee, cocoa, and tomato, among others) considered to be susceptible to this nematode or cultivated in areas with a high incidence of this pathogen. In addition, these two gene families have great potential to be modulated by NBTs in other species of PPNs (e.g., Heterodera schachtii, B. xylophilus, G. pallida, and M. hapla) 13 to develop new strategies for their management and control.…”